Skip to main content

Biochemistry and Physiology of Heavy Metal Resistance and Accumulation in Euglena

  • Chapter
  • First Online:
Euglena: Biochemistry, Cell and Molecular Biology

Abstract

Free-living microorganisms may become suitable models for removal of heavy metals from polluted water bodies, sediments, and soils by using and enhancing their metal accumulating abilities. The available research data indicate that protists of the genus Euglena are a highly promising group of microorganisms to be used in bio-remediation of heavy metal-polluted aerobic and anaerobic acidic aquatic environments. This chapter analyzes the variety of biochemical mechanisms evolved in E. gracilis to resist, accumulate and remove heavy metals from the environment, being the most relevant those involving (1) adsorption to the external cell pellicle; (2) intracellular binding by glutathione and glutathione polymers, and their further compartmentalization as heavy metal-complexes into chloroplasts and mitochondria; (3) polyphosphate biosynthesis; and (4) secretion of organic acids. The available data at the transcriptional, kinetic and metabolic levels on these metabolic/cellular processes are herein reviewed and analyzed to provide mechanistic basis for developing genetically engineered Euglena cells that may have a greater removal and accumulating capacity for bioremediation and recycling of heavy metals.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

β-Ala:

Beta-alanine

Cd-HMWC:

High molecular weight complexes of thiol-molecules with Cd2+

Cd-LMWC:

Low molecular weight complexes of thiol-molecules with Cd2+

EgPCS:

Phytochelatin synthase from E. gracilis

ESTs:

Expressed sequence tags

DW:

Dry weight

PCs:

Phytochelatins

PCS:

Phytochelatin synthase

PolyP:

Polyphosphates

References

  • Albergoni V, Piccinni E, Coppellotti O (1980) Response to heavy metals in organisms-I. Excretion and accumulation of physiological and non physiological metals in Euglena gracilis. Comp Biochem Physiol C 67C:121–127

    Article  CAS  PubMed  Google Scholar 

  • Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals-concepts and applications. Chemosphere 91:869–881

    Article  CAS  PubMed  Google Scholar 

  • Altaş L (2009) Inhibitory effect of heavy metals on methane-producing anaerobic granular sludge. J Hazard Mater 162:1551–1556

    Article  PubMed  CAS  Google Scholar 

  • Andreeva NA, Kulakovskaya TV, KulaevI S (2004) Purification and properties of exopolyphosphatase from the cytosol of Saccharomyces cerevisiae not encoded by the PPX1 gene. Biochemistry (Mosc) 69:387–393

    Article  CAS  Google Scholar 

  • Areco MM, Hanela S, Duran J, Afonso Mdos S (2012) Biosorption of Cu(II), Zn(II), Cd(II) and Pb(II) by dead biomasses of green alga Ulva lactuca and the development of a sustainable matrix for adsorption implementation. J Hazard Mater 213–214:123–132

    Article  PubMed  CAS  Google Scholar 

  • Auger C, Han S, Appanna VP, Thomas SC, Ulibarri G, Appanna VD (2013) Metabolic reengineering invoked by microbial systems to decontaminate aluminum: implications for bioremediation technologies. Biotechnol Adv 31:266–273

    Article  CAS  PubMed  Google Scholar 

  • Avilés C, Loza-Tavera H, Terry N, Moreno-Sánchez R (2003) Mercury pretreatment selects an enhanced cadmium-accumulating phenotype in Euglena gracilis. Arch Microbiol 180:1–10

    Article  PubMed  CAS  Google Scholar 

  • Avilés C, Torres-Márquez ME, Mendoza-Cózatl D, Moreno-Sánchez R (2005) Time-curse development of the Cd2+ hyper-accumulating phenotype in Euglena gracilis. Arch Microbiol 184:83–92

    Article  PubMed  CAS  Google Scholar 

  • Bachhawat AK, Thakur A, Kaur J, Zulkifli M (2013) Glutathione transporters. Biochim Biophys Acta 1830:3154–3164

    Article  CAS  PubMed  Google Scholar 

  • Baker BJ, Banfield JF (2003) Microbial communities in acid mine drainage. FEMS Microbiol Ecol 44:139–152

    Article  CAS  PubMed  Google Scholar 

  • Belcastro M, Marino T, Russo N, Toscano M (2009) The role of glutathione in cadmium ion detoxification: coordination modes and binding properties—a density functional study. J Inorg Biochem 103:50–57

    Article  CAS  PubMed  Google Scholar 

  • Bhargava A, Carmona FF, Bhargava M, Srivastava S (2012) Approaches for enhanced phytoextraction of heavy metals. J Environ Manag 105:103–120

    Article  CAS  Google Scholar 

  • Bi Y, Hubbard C, Purushotham P, Zimmer J (2015) Insights into the structure and function of membrane-integrated processive glycosyltransferase. Curr Opin Struct Biol 34:78–86

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bolchi A, Petrucco S, Tenca PL, Foroni C, Ottonello S (1999) Coordinate modulation of maize sulfate permease and ATP sulfurylase mRNAs in response to variations in sulfur nutrition status: stereospecific down-regulation by L-cysteine. Plant Mol Biol 39:527–537

    Article  CAS  PubMed  Google Scholar 

  • Brake SS, Dannelly HK, Connors KA, Hasiotis ST (2001) Influence of water chemistry on the distribution of an acidophilic protozoan in an acid mine drainage system at the abandoned Green Valley coal mine, Indiana, USA. Appl Geochem 16:1641–1652

    Article  CAS  Google Scholar 

  • Bräutigam A, Schaumlöffel D, Preud’homme H, Thondorf I, Wesenberg D (2011) Physiological characterization of cadmium-exposed Chlamydomonas reinhardtii. Plant Cell Environ 34:2071–2082

    Article  PubMed  CAS  Google Scholar 

  • Brekken DL, Phillips MA (1998) Trypanosoma brucei gamma-glutamylcysteine synthetase. Characterization of the kinetic mechanism and the role of Cys-319 in cystamine inactivation. J Biol Chem 273:26317–26322

    Article  CAS  PubMed  Google Scholar 

  • Breton A, Surdin-Kerjan Y (1977) Sulfate uptake in Saccharomyces cerevisiae: biochemical and genetic study. J Bacteriol 132:224–232

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brito EM, De la Cruz Barrón M, Caretta CA, Goñi-Urriza M, Andrade LH, Cuevas-Rodríguez G, Malm O, Torres JP, Simon M, Guyoneaud R (2015) Impact of hydrocarbons, PCBs and heavy metals on bacterial communities in Lerma River, Salamanca, Mexico: investigation of hydrocarbon degradation potential. Sci Total Environ 521–522:1–10

    Article  PubMed  CAS  Google Scholar 

  • Brooks RR, Chambers MF, Nicks LJ, Robinson BH (1998) Phytomining. Trends Plant Sci 3:359–362

    Article  Google Scholar 

  • Brown JF, Jones DS, Mills DB, Macalady JL, Burgos WD (2011) Application of a depositional Facies model to an acid mine drainage site. Appl Environ Microbiol 77:545–554

    Article  CAS  PubMed  Google Scholar 

  • Brunetti P, Zanella L, Proia A, De Paolis A, Falasca G, Altamura MM, Sanità di Toppi L, Costantino P, Cardarelli M (2011) Cadmium tolerance and phytochelatin content of Arabidopsis seedlings over-expressing the phytochelatin synthase gene AtPCS1. J Exp Bot 62:5509–5519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buetow DE (1962) Differential effects of temperature on the growth of Euglena gracilis. Exp Cell Res 27:137–142

    Article  CAS  PubMed  Google Scholar 

  • Cao MJ, Wang Z, Wirtz M, Hell R, Oliver DJ, Xiang CB (2013) SULTR3;1 is a chloroplast-localized sulfate transporter in Arabidopsis thaliana. Plant J 73:607–616

    Article  CAS  PubMed  Google Scholar 

  • Casiot C, Bruneel O, Personé JC, Leblanc M, Elbaz-Poulichet F (2004) Arsenic oxidation and bioaccumulation by the acidophilic protozoan Euglena mutabilis, in acidic mine drainage (Carnoulès, France). Sci Total Environ 320:259–267

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Zhou J, Goldsbrough PB (1997) Characterization of phytochelatin synthase from tomato. Physiol Plant 101:165–172

    Article  CAS  Google Scholar 

  • Chen HC, Newton AJ, Melis A (2005) Role of SulP, a nuclear-encoded chloroplast sulfate permease, in sulfate transport and H2 evolution in Chlamydomonas reinhardtii. Photosynth Res 84:289–296

    Article  CAS  PubMed  Google Scholar 

  • Ciaffi M, Paolacci AR, Celletti S, Catarcione G, Kopriva S, Astolfi S (2013) Transcriptional and physiological changes in the S assimilation pathway due to single or combined S and Fe deprivation in durum wheat (Tricum durum L.) seedlings. J Exp Bot 64:1663–1675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clemens S, Kim EJ, Neumann D, Schroeder JI (1999) Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J 18:3325–3333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clemente MR, Bustos-Sanmamed P, Loscos J, James EK, Pérez-Rontomé C, Navascués J, Gay M, Becana M (2012) Thiol synthetases of legumes: immunogold localization and differential gene regulation by phytohormones. J Exp Bot 63:3923–3934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Das BK, Roy A, Koschorreck M, Mandal SM, Wendt-Potthoff K, Bhattacharya J (2009) Occurrence and role of algae and fungi in acid mine drainage environment with special reference to metals and sulfate immobilization. Water Res 43:883–894

    Article  CAS  PubMed  Google Scholar 

  • Davis JS, Balinsky JB, Harington JS, Shepherd JB (1973) Assay, purification, properties and mechanism of action of gamma-glutamylcysteine synthetase from the liver of the rat and Xenopus laevis. Biochem J 133:667–678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delalande O, Desvaux H, Godat E, Valleix A, Junot C, Labarre J, Boulard Y (2010) Cadmium-glutathione solution structures provide new insights into heavy metal detoxification. FEBS J 277:5086–5096

    Article  CAS  PubMed  Google Scholar 

  • Deponte M (2013) Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes. Biochim Biophys Acta 1830:3217–3266

    Article  CAS  PubMed  Google Scholar 

  • Devars S, Avilés C, Cervantes C, Moreno-Sánchez R (2000) Mercury uptake and removal by Euglena gracilis. Arch Microbiol 174:175–180

    Article  CAS  PubMed  Google Scholar 

  • Dobáková E, Flegontov P, Skalický T, Lukeš J (2015) Unexpectedly streamlined mitochondrial genome of the euglenozoan Euglena gracilis. Genome Biol Evol 7:3358–3367

    Article  PubMed  PubMed Central  Google Scholar 

  • Docampo R, Moreno SN (2008) The acidocalcisome as a target for chemotherapeutic agents in protozoan parasites. Curr Pharm Des 14:882–888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dorčák V, Kręźel A (2003) Correlation of acid-base chemistry of phytochelatin PC2 with its coordination properties towards the toxic metal ion Cd(II). Dalton Trans 11:2254–2259

    Google Scholar 

  • Dos Santos Ferreira V, Rochetta I, Conforti V, Bench S, Feldman R, Levin MJ (2007) Gene expression patterns in Euglena gracilis: insights into the cellular response to environmental stress. Gene 389:136–145

    Article  CAS  PubMed  Google Scholar 

  • Einicker-Lamas M, Mezian GA, Fernandes TB, Silva FL, Guerra F, Miranda K, Attias M, Oliveira MM (2002) Euglena gracilis as a model for the study of Cu2+ and Zn2+ toxicity and accumulation in eukaryotic cells. Environ Pollut 120:779–786

    Article  CAS  PubMed  Google Scholar 

  • Fang J, Ruiz FA, Docampo M, Lou S, Rodrigues JC, Motta LS, Rohloff P, Docampo R (2007) Overexpression of the Zn2+-sensitive soluble exopolyphosphatase from Trypanosoma cruzi depletes polyphosphates and affects osmoregulation. J Biol Chem 282:32501–32510

    Article  CAS  PubMed  Google Scholar 

  • Frendo P, Harrison J, Norman C, Hernandez Jimenez MJ, Van de Sype G, Gilabert A, Puppo A (2005) Glutathione and homoglutathione play a critical role in the nodulation process of Medicago truncatula. Mol Plant-Microbe Interact 18:254–259

    Article  CAS  PubMed  Google Scholar 

  • Gao Y, Schofield OM, Leustek T (2000) Characterization of sulfate assimilation in marine algae focusing on the enzyme 5′-adenylylsulfate reductase. Plant Physiol 123:1087–1096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • García-García JD, Rodríguez-Zavala JS, Jasso-Chávez R, Mendoza-Cózatl D, Moreno-Sánchez R (2009) Chromium uptake, retention and reduction in photosynthetic Euglena gracilis. Arch Microbiol 191:431–440

    Article  PubMed  CAS  Google Scholar 

  • García-García JD, Olin-Sandoval V, Saavedra E, Girard L, Hernández G, Moreno-Sánchez R (2012) Sulfate uptake in photosynthetic Euglena gracilis. Mechanisms of regulation and contribution to cysteine homeostasis. Biochim Biophys Acta 1820:1567–1575

    Article  PubMed  CAS  Google Scholar 

  • García-García JD, Girard L, Hernández G, Saavedra E, Pardo JP, Rodríguez-Zavala JS, Encalada R, Reyes-Prieto A, Mendoza-Cózatl DG, Moreno-Sánchez R (2014) Zn-bis-glutathionate is the best co-substrate of the monomeric phytochelatin synthase from the photosynthetic heavy metal-hyperaccumulator Euglena gracilis. Metallomics 6:604–616

    Article  PubMed  CAS  Google Scholar 

  • García-García JD, Sánchez-Thomas R, Moreno-Sánchez R (2016) Bio-recovery of non-essential heavy metals by intra- and extracellular mechanisms in free-living microorganisms. Biotechnol Adv 34:859–873

    Article  PubMed  CAS  Google Scholar 

  • Garlaschi FM, Garlaschi A, Lombardi A, Forti G (1974) Effect of ethanol on the metabolism of Euglena gracilis. Plant Sci Lett 2:29–39

    Article  CAS  Google Scholar 

  • Gekeler W, Grill E, Winnacker EL, Zenk MH (1988) Algae sequester heavy metals via synthesis of phytochelatin complexes. Arch Microbiol 150:197–202

    Article  CAS  Google Scholar 

  • Gillet S, Decottignies P, Chardonnet S, Le Maréchal P (2006) Cadmium response and redoxin targets in Chlamydomonas reinhardtii: a proteomic approach. Photosynth Res 89:201–211

    Article  CAS  PubMed  Google Scholar 

  • Graz M, Jarosz-Wilkołazka A, Pawlikowska-Pawlega B (2009) Abortiporus biennis tolerance to insoluble metal oxides: oxalate secretion, oxalate oxidase activity, and mycelial morphology. Biometals 22:401–410

    Article  CAS  PubMed  Google Scholar 

  • Grill E, Winnacker EL, Zenk MH (1985) Phytochelatins: the principal heavy-metal complexing peptides of higher plants. Science 230:674–676

    Article  CAS  PubMed  Google Scholar 

  • Grill E, Loffler S, Winnacker EL, Zenk MH (1989) Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific gamma-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc Natl Acad Sci U S A 86:6838–6842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gutiérrez RL, Rubio-Arias H, Quintana R, Ortega JA, Gutierrez M (2008) Heavy metals in water of the San Pedro River in Chihuahua, Mexico and its potential health risk. Int J Environ Res Public Health 5:91–98

    Article  PubMed  PubMed Central  Google Scholar 

  • Ha SB, Smith AP, Howden R, Dietrich WM, Bugg S, O’Connell MJ, Goldsbrough PB, Cobbett CS (1999) Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. Plant Cell 11:1153–1164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hallick RB, Hong L, Drager RG, Favreau MR, Monfort A, Orsat B, Spielmann A, Stutz E (1993) Complete sequence of Euglena gracilis chloroplast DNA. Nucleic Acids Res 21:3537–3544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Halter D, Casiot C, Heipieper HJ, Plewniak F, Marchal M, Simon S, Arsène-Ploetze F, Bertin PN (2012a) Surface properties and intracellular speciation revealed an original adaptive mechanism to arsenic in the acid mine drainage bio-indicator Euglena mutabilis. Appl Microbiol Biotechnol 93:1735–1744

    Article  CAS  PubMed  Google Scholar 

  • Halter D, Goulhen-Chollet F, Gallien S, Casiot C, Hamelin J, Gilard F, Heintz D, Schaeffer C, Carapito C, van Dorsselaer A, Tcherkez G, Arsène-Ploetze F, Bertin PN (2012b) In situ proteo-metabolomics reveals metabolite secretion by the acid mine drainage bio-indicator, Euglena mutabilis. ISME J 6:1391–1402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanna E, Ng KF, MacRae IJ, Bley CJ, Fisher AJ, Segel IH (2004) Kinetic and stability properties of Penicillium chrysogenum ATP sulfurylase missing the C-terminal regulatory domain. J Biol Chem 279:4415–4424

    Article  CAS  PubMed  Google Scholar 

  • Hargreaves JW, Lloyd EJH, Whitton BA (1975) Chemistry and vegetation of highly acidic streams. Freshw Biol 5:563–576

    Article  Google Scholar 

  • Hashim MA, Mukhopadhyay S, Sahu JN, Sengupta B (2011) Remediation technologies for heavy metal contaminated groundwater. J Environ Manag 92:2355–2388

    Article  CAS  Google Scholar 

  • Hawes CS, Nicholas DJ (1973) Adenosine 5′-Triphosphate sulfurylase from Saccharomyces cerevisiae. Biochem J 133:541–550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hell R, Bergmann L (1990) γ-Glutamylcysteine synthetase in higher plants: catalytic properties and subcellular localization. Planta 180:603–612

    Article  CAS  PubMed  Google Scholar 

  • Hirata K, Tsujimoto Y, Namba T, Ohta T, Hirayanagi N, Miyasaka H, Zenk MH, Miyamoto K (2001) Strong induction of phytochelatin synthesis by zinc in marine green alga Dunaliella tertiolecta. J Biosci Bioeng 92:24–29

    Article  CAS  PubMed  Google Scholar 

  • Hu G, Bi S, Xu G, Zhang Y, Mei X, Li A (2015) Distribution and assessment of heavy metals off the Changjiang River mouth and adjacent area during the past century and the relationship of the heavy metals with anthropogenic activity. Mar Pollut Bull 96:434–440

    Article  CAS  PubMed  Google Scholar 

  • Huang J, Nkrumah PN, Anim DO, Mensah E (2014) E-waste disposal effects on the aquatic environment: Accra, Ghana. Rev Environ Contam Toxicol 229:19–34

    CAS  PubMed  Google Scholar 

  • Inui H, Miyatake K, Nakano Y, Kitaoka S (1985) The physiological role of oxygen-sensitive pyruvate dehydrogenase in mitochondrial fatty acid synthesis in Euglena gracilis. Arch Biochem Biophys 237:423–429

    Article  CAS  PubMed  Google Scholar 

  • Inui H, Ono K, Miyatake K, Nakano Y, Kitaoka S (1987) Purification and characterization of pyruvate:NADP+ oxidoreductase in Euglena gracilis. J Biol Chem 262:9130–9135

    CAS  PubMed  Google Scholar 

  • Inui H, Miyatake K, Nakano Y, Kitaoka S (1990) Pyruvate:NADP+ oxidoreductase from Euglena gracilis: mechanism of O2-inactivation of the enzyme and its stability in the aerobe. Arch Biochem Biophys 280:292–298

    Article  CAS  PubMed  Google Scholar 

  • Ishii N, Uchida S (2006) Removal of technetium from solution by algal flagellate Euglena gracilis. J Environ Qual 35:2017–2020

    Article  CAS  PubMed  Google Scholar 

  • Ivušić F, Šantek B (2015) Optimization of complex medium composition for heterotrophic cultivation of Euglena gracilis and paramylon production. Bioprocess Biosyst Eng 38:1103–1112

    Article  PubMed  CAS  Google Scholar 

  • Jamers A, Blust R, De Coen W, Griffin JL, Jones OA (2013) An omics based assessment of cadmium toxicity in the green alga Chlamydomonas reinhardtii. Aquat Toxicol 126:355–364

    Article  CAS  PubMed  Google Scholar 

  • Jarosz-Wilkołazka A, Graz M, Braha B, Menge S, Schlosser D, Krauss GJ (2006) Species-specific Cd-stress response in the white rot basidiomycetes Abortiporus biennis and Cerrena unicolor. Biometals 19:39–49

    Article  PubMed  CAS  Google Scholar 

  • Jasso-Chávez R, Moreno-Sánchez R (2003) Cytosol-mitochondria transfer of reducing equivalents by a lactate shuttle in heterotrophic Euglena. Eur J Biochem 270:4942–4951

    Article  PubMed  CAS  Google Scholar 

  • Jasso-Chávez R, Pacheco-Rosales A, Lira-Silva E, Gallardo-Pérez JC, García N, Moreno-Sánchez R (2010) Toxic effects of Cr(VI) and Cr(III) on energy metabolism of heterotrophic Euglena gracilis. Aquat Toxicol 100:329–338

    Article  PubMed  CAS  Google Scholar 

  • Jensen A, Bro-Rasmunssen F (1992) Environment cadmium in Europe. Rev Environ Contam Toxicol 125:101–181

    CAS  PubMed  Google Scholar 

  • Kataoka T, Watanabe-Takahashi A, Hayashi N, Ohnishi M, Mimura T, Buchner P, Hawkesford MJ, Yamaya T, Takahashi H (2004) Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell 16:2693–2704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keasling JD (1997) Regulation of intracellular toxic metals and other cations by hydrolysis of polyphosphate. Ann N Y Acad Sci 829:242–249

    Article  CAS  PubMed  Google Scholar 

  • Keasling JD, Hupf GA (1996) Genetic manipulation of polyphosphate metabolism affects cadmium tolerance in Escherichia coli. Appl Environ Microbiol 62:743–746

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi K, Yoshimoto A (1982) Studies on yeast sulfite reductase. IV. Structure and steady-state kinetics. Biochim Biophys Acta 705:348–356

    Article  CAS  PubMed  Google Scholar 

  • Kondo N, Isobe M, Imai K, Goto T (1983) Structure of cadystin, the unit-peptide of cadmium-binding peptides induced in a fission yeast, Schizosaccharomyces pombe. Tetrahedron Lett 24:925–928

    Article  CAS  Google Scholar 

  • Kopriva S (2006) Regulation of sulfate assimilation in Arabidopsis and beyond. Ann Bot 97:479–495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koprivova A, Kopriva S (2014) Molecular mechanisms of reguation of sulfate assimilation: first steps on a long road. Front Plant Sci 5:589

    Article  PubMed  PubMed Central  Google Scholar 

  • Lancilli C, Giacomini B, Lucchini G, Davidian JC, Cocucci M, Sacchi GA, Nocito FF (2014) Cadmium exposure and sulfate limitation reveal differences in the transcriptional control of three sulfate transport (Sultr1;2) genes in Brassica juncea. BMC Plant Biol 14:132

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lappartient AG, Touraine B (1996) Demand-driven control of root ATP sulfurylase activity and SO4 2- uptake in intact canola (the role of phloem-translocated glutathione). Plant Physiol 111:147–157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lappartient AG, Vidmar JJ, Leustek T, Glass AD, Touraine B (1999) Inter-organism signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound. Plant J 18:89–95

    Article  CAS  PubMed  Google Scholar 

  • Lee DC, Park CJ, Yang JE, Jeong YH, Rhee HI (2000) Screening of hexavalent chromium biosorbent from marine algae. Appl Microbiol Biotechnol 54:597–600

    Article  CAS  PubMed  Google Scholar 

  • Lemercier G, Espiau B, Ruiz FA, Vieira M, Luo S, Baltz T, Docampo R, Bakalara N (2004) A pyrophosphatase regulating polyphosphate metabolism in acidocalcisomes is essential for Trypanosoma brucei virulence in mice. J Biol Chem 279:3420–3425

    Article  CAS  PubMed  Google Scholar 

  • León J, Romero LC, Galván F, Vega JM (1987) Purification and physicochemical characterization of O-acetyl-L-serine sulfhydrylase from Chlamydomonas reinhardtii. Plant Sci 53:93–99

    Article  Google Scholar 

  • Levinson SL, Jacobs LH, Krulwich TA, Li HC (1975) Purification and characterization of a polyphosphate kinase from Arthrobacter atrocyaneus. J Gen Microbiol 88:65–74

    Article  Google Scholar 

  • Li JJ, Saidha T, Schiff JA (1991) Purification and properties of two forms of ATP sulfurylase from Euglena. Biochim Biophys Acta 1078:68–76

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Dhankher OP, Carreira L, Lee D, Chen A, Schroeder JI, Balish RS, Meagher RB (2004) Overexpression of phytochelatin synthase in Arabidopsis leads to enhanced arsenic tolerance and cadmium hypersensitivity. Plant Cell Physiol 45:1787–1797

    Article  CAS  PubMed  Google Scholar 

  • Linder SN, Vidaurre D, Willbold S, Schoberth SM, Wendisch VF (2007) NCgl2620 encodes a class II polyphosphate kinase in Corynebacterium glutamicum. Appl Environ Microbiol 73:5026–5033

    Article  CAS  Google Scholar 

  • Lira-Silva E, Ramírez-Lima IS, Olín-Sandoval V, García-García JD, García-Contreras R, Moreno-Sánchez R, Jasso-Chávez R (2011) Removal, accumulation and resistance to chromium in heterotrophic Euglena gracilis. J Hazard Mater 193:216–224

    Article  CAS  PubMed  Google Scholar 

  • Lira-Silva E, Santiago-Martínez MG, García-Contreras R, Zepeda-Rodríguez A, Marín-Hernández A, Moreno-Sánchez R, Jasso-Chávez R (2013) Cd2+ resistance mechanisms in Methanosarcina acetivorans involve the increase in the coenzyme M content and induction of biofilm synthesis. Environ Microbiol Rep 5:799–808

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Wu FH, Li JX, Chen J, Wang GH, Wang WH, Hu WJ, Gao LJ, Wang ZL, Chen JH, Simon M, Zheng HL (2016) Glutathione homeostasis and Cd tolerance in the Arabidopsis sultr1;1-sultr1;2 double mutant with limiting sulfate supply. Plant Cell Rep 35:397–413

    Article  CAS  PubMed  Google Scholar 

  • Lu SC (2013) Glutathione synthesis. Biochim Biophys Acta 1830:3143–3453

    Article  CAS  PubMed  Google Scholar 

  • Lueder DV, Phillips MA (1996) Characterization of Trypanosoma brucei gamma-glutamylcysteine synthetase, an essential enzyme in the biosynthesis of trypanothione (diglutathionylspermidine). J Biol Chem 271:17485–17490

    Article  CAS  PubMed  Google Scholar 

  • Luís AT, Teixeira P, Almeida SF, Matos JX, da Silva EF (2011) Environmental impact of mining activities in the Lousal area (Portugal): chemical and diatom characterization of metal-contaminated stream sediments and surface water of Corona stream. Sci Total Environ 409:4312–4325

    Article  PubMed  CAS  Google Scholar 

  • Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278

    Article  CAS  PubMed  Google Scholar 

  • Marentes E, Rauser WE (2007) Different proportions of cadmium occur as Cd-binding phytochelatin complexes in plants. Physiol Plant 131:291–301

    CAS  PubMed  Google Scholar 

  • Maruyama-Nakashita A, Watanabe-Takahashi A, Inoue E, Yamaya T, Saito K, Takahashi H (2015) Sulfur-responsive elements in the 3′-nontranscribed intergenic region are essential for the induction of sulfate transporter 2;1 gene expression in Arabidopsis roots sulfur deficiency. Plant Cell 27:1279–1296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mata YN, Blazquez ML, Ballester A, González F, Muñoz JA (2009a) Biosorption of cadmium, lead and copper with calcium alginate xerogels and immobilized Fucus vesiculosus. J Hazard Mater 163:555–562

    Article  CAS  PubMed  Google Scholar 

  • Mata YN, Torres E, Blázquez ML, Ballester A, González F, Muñoz JA (2009b) Gold(III) biosorption and bioreduction with the brown alga Fucus vesiculosus. J Hazard Mater 166:612–618

    Article  CAS  PubMed  Google Scholar 

  • Matamoros MA, Moran JF, Iturbe-Ormaetxe I, Rubio MC, Becana M (1999) Glutathione and homoglutathione synthesis in legume root nodules. Plant Physiol 121:879–888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsuda YC, Colman B (1995) Characterization of sulfate transport in the green alga Chlorella ellipsoidea. Plant Cell Physiol 36:1291–1296

    CAS  Google Scholar 

  • Matsuda F, Hayashi M, Kondo A (2011) Comparative profiling analysis of central metabolites in Euglena gracilis under various cultivation conditions. Biosci Biotechnol Biochem 75:2253–2256

    Article  CAS  PubMed  Google Scholar 

  • McComb JQ, Han FX, Rogers C, Thomas C, Arslan Z, Ardeshir A, Tchounwou PB (2015) Trace elements and heavy metals in the Gran Bay National Estuarine Reserve in the northern Gulf of Mexico. Mar Pollut Bull 99:61–69

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mehta SK, Gaur JP (2005) Use of algae for removing heavy metal ions from wastewater: progress and prospects. Crit Rev Biotechnol 25:113–152

    Article  CAS  PubMed  Google Scholar 

  • Mendoza-Cózatl DG, Moreno-Sánchez R (2006) Control of glutathione and phytochelatin synthesis under cadmium stress. Pathway modeling for plants. J Theor Biol 238:919–936

    Article  PubMed  CAS  Google Scholar 

  • Mendoza-Cózatl D, Devars S, Loza-Tavera H, Moreno-Sánchez R (2002) Cadmium accumulation in the chloroplast of Euglena gracilis. Physiol Plant 115:276–283

    Article  PubMed  Google Scholar 

  • Mendoza-Cózatl D, Loza-Tavera H, Hernández-Navarro A, Moreno-Sánchez R (2005) Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants. FEMS Microbiol Rev 29:653–671

    Article  PubMed  CAS  Google Scholar 

  • Mendoza-Cózatl DG, Rangel-González E, Moreno-Sánchez R (2006a) Simultaneous Cd2+, Zn2+, and Pb2+ uptake and accumulation by photosynthetic Euglena gracilis. Arch Environ Contam Toxicol 51:521–528

    Article  PubMed  CAS  Google Scholar 

  • Mendoza-Cózatl DG, Rodríguez-Zavala JS, Rodríguez-Enríquez S, Mendoza-Hernandez G, Briones-Gallardo R, Moreno-Sánchez R (2006b) Phytochelatin-cadmium-sulfide high-molecular-mass complexes of Euglena gracilis. FEBS J 273:5703–5713

    Article  PubMed  CAS  Google Scholar 

  • Mendoza-Cózatl DG, Zhai Z, Jobe TO, Akmakjian GZ, Song WY, Limbo O, Russell MR, Kozlovskyy VI, Martinoia E, Vatamaniuk OK, Russell P, Schroeder JI (2010) Tonoplast-localized Abc2 transporter mediates phytochelatin accumulation in vacuoles and confers cadmium tolerance. J Biol Chem 285:40416–40426

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mendoza-Cózatl DG, Jobe TO, Hauser F, Schroeder JI (2011) Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic. Curr Opin Plant Biol 14:554–562

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Millard P, Evans LV (1982) Sulphate uptake in the unicellular marine red alga Rhodella maculata. Arch Microbiol 131:165–169

    Article  CAS  Google Scholar 

  • Miot J, Morin G, Skouri-Panet F, Férard C, Aubry E, Briand J, Wang Y, Ona-Nguema G, Guyot F, Brown GE (2008) XAS study of arsenic coordination in Euglena gracilis exposed to arsenite. Environ Sci Technol 42:5342–5347

    Article  CAS  PubMed  Google Scholar 

  • Moreno-Sánchez R, Covián R, Jasso-Chávez R, Rodríguez-Enríquez S, Pacheco-Moisés F, Torres-Márquez ME (2000) Oxidative phosphorylation supported by an alternative respiratory pathway in mitochondria from Euglena. Biochim Biophys Acta 1457:200–210

    Article  PubMed  Google Scholar 

  • Moreno-Sánchez R, Saavedra E, Gallardo-Pérez JC, Rumjanek FD, Rodríguez-Enríquez S (2016) Understanding the cancer cell phenotype beyond the limitations of current omics analyses. FEBS J 283:54–73

    Article  PubMed  CAS  Google Scholar 

  • Murphy V, Hughes H, McLoughlin P (2008) Comparative study of chromium biosorption by red, green and brown seaweed biomass. Chemosphere 70:1128–1134

    Article  CAS  PubMed  Google Scholar 

  • Nagalakshmi N, Prasad MN (2001) Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160:291–299

    Article  CAS  PubMed  Google Scholar 

  • Nagata T, Ishikawa C, Kiyono M, Pan-Hou H (2006) Accumulation of mercury in transgenic tobacco expressing bacterial polyphosphate. Biol Pharm Bull 29:2350–2353

    Article  CAS  PubMed  Google Scholar 

  • Nagata T, Kimura T, Pan-Hou H (2008) Engineering expression of polyphosphate confers cadmium resistance in tobacco. J Toxicol Sci 33:371–373

    Article  CAS  PubMed  Google Scholar 

  • Nagel K, Adelmeier U, Voigt J (1996) Subcellular distribution of cadmium in the unicellular green alga Chlamydomonas reinhardtii. J Plant Physiol 149:86–90

    Article  CAS  Google Scholar 

  • Nakagawa CW, Mutoh N, Hayashi Y (1993) Glutathione synthetase from the fission yeast. Purification and its unique heteromeric subunit structure. Biochem Cell Biol 71:447–453

    Article  CAS  PubMed  Google Scholar 

  • Nakano Y, Urade Y, Urade R, Kitaoka S (1987) Isolation, purification and characterization of the pellicle of Euglena gracilis z. J Biochem 102:1053–1063

    Article  CAS  PubMed  Google Scholar 

  • Nam SH, Lee WN, Shin YJ, Yoon SJ, Kim SW, Kwak JI, An YJ (2014) Derivation of guideline values for gold (III) ion toxicity limits to protect aquatic ecosystems. Water Res 48:126–136

    Article  CAS  PubMed  Google Scholar 

  • Nancucheo I, Johnson DB (2012) Acidophilic algae isolated from mine-impacted environments and their roles in sustaining heterotrophic acidophiles. Front Microbiol 3:325

    Article  PubMed  PubMed Central  Google Scholar 

  • Nefedova Y, Fishman M, Sherman S, Wang X, Beg AA, Gabrilovich DI (2007) Mechanism of all-trans retinoic acid effect on tumor-associated myeloid-derived suppressor cells. Cancer Res 67:11021–11028

    Article  CAS  PubMed  Google Scholar 

  • Nicolas P, Freyssinet G, Nigon V (1980) Effect of light on glucose utilization by Euglena gracilis. Plant Physiol 65:631–634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishikawa K, Onodera A, Tominaga N (2006) Phytochelatins do not correlate with the level of Cd accumulation in Chlamydomonas spp. Chemosphere 63:1553–1559

    Article  CAS  PubMed  Google Scholar 

  • Nocito FF, Lancilli C, Crema B, Fourcroy P, Davidian JC, Sacchi GA (2006) Heavy metal stress and sulfate uptake in maize roots. Plant Physiol 141:1138–1148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Neill EC, Trick M, Hill L, Rejzek M, Dusi RG, Hamilton CJ, Zimba PV, Henrissat B, Field RA (2015) The transcriptome of Euglena gracilis reveals unexpected metabolic capabilities for carbohydrate and natural product biochemistry. Mol Biosyst 11:2808–2820

    Article  PubMed  CAS  Google Scholar 

  • Olaveson MM, Nalewajko C (2000) Effects of acidity on the growth of two Euglena species. Hydrobiologia 433:39–56

    Article  CAS  Google Scholar 

  • Olin-Sandoval V, González-Chávez Z, Berzunza-Cruz M, Martínez I, Jasso-Chávez R, Becker I, Espinoza B, Moreno-Sánchez R, Saavedra E (2012) Drug target validation of the trypanothione pathway enzymes through metabolic modelling. FEBS J 279:1811–1833

    Article  CAS  PubMed  Google Scholar 

  • Orell A, Navarro CA, Rivero M, Aguilar JS, Jerez CA (2012) Inorganic polyphosphates in extremophiles and their possible functions. Extremophiles 16:573–583

    Article  CAS  PubMed  Google Scholar 

  • Ortiz DF, Kreppel L, Speiser DM, Scheel G, McDonald G, Ow DW (1992) Heavy metal tolerance in the fission yeast requires an ATP-binding cassette-type vacuolar membrane transporter. EMBO J 11:3491–3499

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ortiz DF, Ruscitti T, McCue KF, Ow DW (1995) Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. J Biol Chem 270:4721–4728

    Article  CAS  PubMed  Google Scholar 

  • Osaki Y, Shirabe T, Nakanishi H, Wakagi T, Yoshimura E (2009) Characterization of phytochelatin synthase produced by the primitive red alga Cyanidioschyzon merolae. Metallomics 1:353–358

    Article  CAS  PubMed  Google Scholar 

  • Oven M, Page JE, Zenk MH, Kutchan TM (2002) Molecular characterization of the homo-phytochelatin synthase of soybean Glycine max: relation to phytochelatin synthase. J Biol Chem 277:4747–4754

    Article  CAS  PubMed  Google Scholar 

  • Park H, Bakalinsky AT (2000) SSU1 mediates sulphite efflux in Saccharomyces cerevisiae. Yeast 16:881–888

    Article  CAS  PubMed  Google Scholar 

  • Patron NJ, Durnford DG, Kopriva S (2008) Sulfate assimilation in eukaryotes: fusions, relocations and lateral transfers. BMC Evol Biol 8:39

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Paul D, Pandey G, Pandey J, Jain RK (2005) Accessing microbial diversity for bioremediation and environmental restoration. Trends Biotechnol 23:135–142

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Castiñeira JR, Gómez-García R, López-Marqués RL, Losada M, Serrano A (2001) Enzymatic systems of inorganic pyrophosphate bioenergetics in photosynthetic and heterotrophic protists: remnants or metabolic cornerstones? Int Microbiol 4:135–142

    PubMed  Google Scholar 

  • Phartiyal P, Kim WS, Cahoon RE, Jez JM, Krishnan HB (2006) Soybean ATP sulfurylase, a homodimeric enzyme involved in sulfur assimilation, is abundantly expressed in roots and induced by cold treatment. Arch Biochem Biophys 450:20–29

    Article  CAS  PubMed  Google Scholar 

  • Phartiyal P, Kim WS, Cahoon RE, Jez JM, Krishnan HB (2008) The role of 5′-adenylylsulfate reductase in the sulfur assimilation pathway of soybean: molecular cloning, kinetic characterization, and gene expression. Phytochemistry 69:356–364

    Article  CAS  PubMed  Google Scholar 

  • Prasanna R, Ratha SK, Rojas C, Bruns MA (2011) Algal diversity in flowing waters at an acidic mine drainage “barrens” in central Pennsylvania, USA. Folia Microbiol (Praha) 56:491–496

    Article  CAS  Google Scholar 

  • Preuss ML, Cameron JC, Berg RH, Jez JM (2014) Immunolocalization of glutathione biosynthesis enzymes in Arabidopsis thaliana. Plant Physiol Biochem 75:9–13

    Article  CAS  PubMed  Google Scholar 

  • Proudfoot M, Kuznetsova E, Brown G, Rao NN, Kitagawa M, Mori H, Savchenko A, Yakunin AF (2004) General enzymatic screens identify three new nucleotidases in Escherichia coli. Biochemical characterization of SurE, YfbR, and YjjG. J Biol Chem 279:54687–54694

    Article  CAS  PubMed  Google Scholar 

  • Ramos J, Clemente MR, Naya L, Loscos J, Pérez-Rontomé C, Sato S, Tabata S, Becana M (2007) Phytochelatin synthases of the model legume Lotus japonicus. A small multigene family with differential response to cadmium and alternatively spliced variants. Plant Physiol 143:1110–1118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ray D, Williams DL (2011) Characterization of the phytochelatin synthase of Schistosoma mansoni. PLoS Negl Trop Dis 5:e1168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richman PG, Meister A (1975) Regulation of gamma-glutamyl-cysteine synthetase by nonallosteric feedback inhibition by glutathione. J Biol Chem 250:1422–1426

    CAS  PubMed  Google Scholar 

  • Rigouin C, Nylin E, Cogswell AA, Schaumlöffel D, Dobritzsch D, Williams DL (2013) Towards an understanding of the function of the phytochelatin synthase of Schistosoma mansoni. PLoS Negl Trop Dis 7:e2037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson BH, Leblanc M, Petit D, Brooks RR, Kirkman JH, Gregg PEH (1998) The potential of Thlaspi caerulescens for phytoremediation of contaminated soils. Plant Soil 203:47–56

    Article  CAS  Google Scholar 

  • Rocchetta I, Mazzuca M, Conforti V, Ruiz L, Balzaretti V, Rios de Molina Mdel C (2006) Effect of chromium on the fatty acid composition of two strains of Euglena gracilis. Environ Pollut 141:353–358

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Zavala JS, Ortiz-Cruz MA, Moreno-Sánchez R (2006) Characterization of an aldehyde dehydrogenase from Euglena gracilis. J Eukaryot Microbiol 53:36–42

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez-Zavala JS, Ortiz-Cruz MA, Mendoza-Hernández G, Moreno-Sánchez R (2010) Increased synthesis of alpha-tocopherol, paramylon and tyrosine by Euglena gracilis under conditions of high biomass production. J Appl Microbiol 109:2160–2172

    Article  PubMed  CAS  Google Scholar 

  • Romero LC, Aroca MÁ, Laureano-Marin AM, Moreno I, Garcia I, Gotor C (2014) Cysteine and cysteine-related signaling pathways in Arabidopsis thaliana. Mol Plant 7:264–276

    Article  CAS  PubMed  Google Scholar 

  • Roncarati F, Sáez CA, Greco M, Gledhill M, Bitonti MB, Brown MT (2015) Response differences between Ectocarpus siliculosus populations to copper stress involve cellular exclusion and induction of the phytochelatin biosynthetic pathway. Aquat Toxicol 159:167–175

    Article  CAS  PubMed  Google Scholar 

  • Ruelas-Inzunza J, Green-Ruiz C, Zavala-Nevárez M, Soto-Jiménez M (2011) Biomonitoring of Cd, Cr, Hg, and Pb in the Baluarte River basin associated to a mining area (NW Mexico). Sci Total Environ 409:3527–3536

    Article  CAS  PubMed  Google Scholar 

  • Ruiz FA, Marchesini N, Seufferheld M, Govindjee, Docampo R (2001) The polyphosphate bodies of Chlamydomonas reinhardtii possess a proton-pumping pyrophosphatase and are similar to acidocalcisomes. J Biol Chem 276:46196–46203

    Article  CAS  PubMed  Google Scholar 

  • Ruiz LB, Rocchetta I, Ferreira VDS, Conforti V (2004) Isolation, culture and characterization of a new strain of Euglena gracilis. Phycol Res 52:168–173

    Article  Google Scholar 

  • Saidha T, Stern AI, Lee DH, Schiff JA (1985) Localization of a sulphate-activating system within Euglena mitochondria. Biochem J 232:357–365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saidha T, Na SQ, Li JY, Schiff JA (1988) A sulphate metabolizing centre in Euglena mitochondria. Biochem J 253(2):533–539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sánchez-Thomas R, Moreno-Sánchez R, García-García JD (2016) Accumulation of zinc protects against cadmium stress in photosynthetic Euglena gracilis. Environ Exp Bot 131:19–31

    Article  CAS  Google Scholar 

  • Šantek B, Friehs K, Lotz M, Flaschel E (2012) Production of paramylon, a β-1,3-glucan, by heterotrophic growth of Euglena gracilis on potato liquor in fed-batch and repeated-batch mode of cultivation. Eng Life Sci 12:89–94

    Article  CAS  Google Scholar 

  • Santiago-Martínez MG, Lira-Silva E, Encalada R, Pineda E, Gallardo-Pérez JC, Zepeda-Rodríguez A, Moreno-Sánchez R, Saavedra E, Jasso-Chávez R (2015) Cadmium removal by Euglena gracilis is enhanced under anaerobic growth conditions. J Hazard Mater 288:104–112

    Article  PubMed  CAS  Google Scholar 

  • Sarmiento AM, DelValls A, Miguel-Nieto J, Salamanca MJ, Caraballo MA (2011) Toxicity and potential risk assessment of a river polluted by acid mine drainage in the Iberian Pyrite Belt (SW Spain). Sci Total Environ 409:4763–4771

    Article  CAS  PubMed  Google Scholar 

  • Sarry JE, Kuhn L, Ducruix C, Lafaye A, Junot C, Hugouvieux V, Jourdain A, Bastien O, Fievet JB, Vailhen D, Amekraz B, Moulin C, Ezan E, Garin J, Bourguignon J (2006) The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics 6:2180–2198

    Article  CAS  PubMed  Google Scholar 

  • Schäfer HJ, Greiner S, Rausch T, Haag-Kerwer A (1997) In seedlings of the heavy metal accumulator Brassica juncea Cu2+ differentially affects transcript amounts for gamma-glutamylcysteine synthetase (gamma-ECS) and metallothionein (MT2). FEBS Lett 404:216–220

    Article  PubMed  Google Scholar 

  • Schäfer HJ, Haag-Kerwer A, Rausch T (1998) cDNA cloning and expression analysis of genes encoding GSH synthesis in roots of the heavy-metal accumulator Brassica juncea L.: evidence for Cd-induction of a putative mitochondrial gamma-glutamylcysteine synthetase isoform. Plant Mol Biol 37:87–97

    Article  PubMed  Google Scholar 

  • Schandle VB, Rudolph FB (1981) Isotope exchange at equilibrium studies with rat kidney gamma-glutamylcysteine synthetase. J Biol Chem 256:7590–7594

    CAS  PubMed  Google Scholar 

  • Scheerer U, Haensch R, Mendel RR, Kopriva S, Rennenberg H, Herschbach C (2010) Sulphur flux through the sulphate assimilation pathway is differently controlled by adenosine 5′-phosphosulphate reductase under stress and in transgenic poplar plants overexpressing gamma-ECS, SO, or APR. J Exp Bot 61:609–622

    Article  CAS  PubMed  Google Scholar 

  • Schneider T, Betz A (1985) Wax monoester fermentation in Euglena gracilis T. Factors favouring the synthesis of odd-numbered fatty acids and alcohols. Planta 166:67–73

    Article  CAS  PubMed  Google Scholar 

  • Sekine K, Sakakibara Y, Hase T, Sato N (2009) A novel variant of ferredoxin-dependent sulfite reductase having preferred substrate specificity for nitrate in the unicellular red alga Cyanidioschyzon merolae. Biochem J 423:91–98

    Article  CAS  PubMed  Google Scholar 

  • Seufferheld M, Curzi MJ (2010) Recent discoveries on the roles of polyphosphates in plants. Plant Mol Biol Report 28:549–559

    Article  CAS  Google Scholar 

  • Shen H, He LF, Sasaki T, Yamamoto Y, Zheng SJ, Ligaba A, Yan XL, Ahn SJ, Yamaguchi SJ, Sasakawa H, Matsumoto H (2005) Citrate secretion coupled with the modulation of soybean root tip under aluminum stress. Up-regulation of transcription, translation, and threonine-oriented phosphorylation of plasma membrane H+-ATPase. Plant Physiol 138:287–296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shum KT, Lui EL, Wong SC, Yeung P, Sam L, Wang Y, Watt RM, Tanner JA (2011) Aptamer-mediated inhibition of Mycobacterium tuberculosis polyphosphate kinase 2. Biochemistry 50:3261–3271

    Article  CAS  PubMed  Google Scholar 

  • Simpson WR (1981) A critical review of cadmium on marine environment. Prog Oceanogr 10:1–70

    Article  Google Scholar 

  • Sittenfeld A, Mora M, Ortega JM, Albertazzi F, Cordero A, Roncel M, Sánchez E, Vargas M, Fernández M, Weckesser J, Serrano A (2002) Characterization of a photosynthetic Euglena strain isolated from an acidic hot mud pool of a volcanic area of Costa Rica. FEMS Microbiol Ecol 42:151–161

    CAS  PubMed  Google Scholar 

  • Sommer JR, Blum JJ (1965) Cytochemical localization of acid phosphatases in Euglena gracilis. J Cell Biol 24:235–251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sooksa-Nguan T, Yakubov B, Kozlovskyy VI, Barkume CM, Howe KJ, Thannhauser TW, Rutzke MA, Hart JJ, Kochian LV, Rea PA, Vatamaniuk OK (2009) Drosophila ABC transporter, DmHMT-1, confers tolerance to cadmium. DmHMT-1 and its yeast homolog, SpHMT-1, are not essential for vacuolar phytochelatin sequestration. J Biol Chem 284:354–362

    Article  CAS  PubMed  Google Scholar 

  • Sun H, Han J, Li D, Zhang S, Lu X (2010) Chemical weathering inferred from riverine water chemistry in the lower Xijiang basin, South China. Sci Total Environ 408:4749–4760

    Article  CAS  PubMed  Google Scholar 

  • Suter M, von Ballmoos P, Kopriva S, den Camp RO, Schaller J, Kuhlemeier C, Schurmann P, Brunold C (2000) Adenosine 5′-phosphosulfate sulfotransferase and adenosine 5′-phosphosulfate reductase are identical enzymes. J Biol Chem 275:930–936

    Article  CAS  PubMed  Google Scholar 

  • Teerawanichpan P, Qiu X (2010) Fatty acyl-CoA reductase and wax synthase from Euglena gracilis in the biosynthesis of medium-chain wax esters. Lipids 45:263–273

    Article  CAS  PubMed  Google Scholar 

  • Trenfield MA, Ng JC, Noller B, Markich SJ, van Dam RA (2012) Dissolved organic carbon reduces uranium toxicity to the unicellular eukaryote Euglena gracilis. Ecotoxicology 21:1013–1023

    Article  CAS  PubMed  Google Scholar 

  • Tsuji N, Hirayanagi N, Iwabe O, Namba T, Tagawa M, Miyamoto S, Miyasaka H, Takagi M, Hirata K, Miyamoto K (2003) Regulation of phytochelatin synthesis by zinc and cadmium in marine green algae, Dunaliella tertiolecta. Phytochemistry 62:453–459

    Article  CAS  PubMed  Google Scholar 

  • Vatamaniuk OK, Mari S, Lu YP, Rea PA (2000) Mechanism of heavy metal ion activation of phytochelatin (PC) synthase: blocked thiols are sufficient for PC synthase-catalyzed transpeptidation of glutathione and related thiol peptides. J Biol Chem 275:31451–31459

    Article  CAS  PubMed  Google Scholar 

  • Vatamaniuk OK, Bucher EA, Ward JT, Rea PA (2001) A new pathway for heavy metal detoxification in animals. Phytochelatin synthase is required for cadmium tolerance in Caenorhabditis elegans. J Biol Chem 276:20817–20820

    Article  CAS  PubMed  Google Scholar 

  • Vatamaniuk OK, Bucher EA, Sundaram MV, Rea PA (2005) CeHMT-1, a putative phytochelatin transporter, is required for cadmium tolerance in Caenorhabditis elegans. J Biol Chem 280:23684–23690

    Article  CAS  PubMed  Google Scholar 

  • Vauclare P, Kopriva S, Fell D, Suter M, Sticher L, von Ballmoos P, Krähenbühl U, den Camp RO, Brunold C (2002) Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5′-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols. Plant J 31:729–740

    Article  CAS  PubMed  Google Scholar 

  • Vázquez-Sauceda ML, Pérez-Castañeda R, Sánchez-Martínez JG, Aguirre-Guzmán G (2012) Cadmium and lead levels along the estuarine ecosystem of Tigre River-San Andres Lagoon, Tamaulipas, Mexico. Bull Environ Contam Toxicol 89:782–785

    Article  CAS  Google Scholar 

  • Venkata Mohan S, Rohit MV, Chirajeevi P, Chandra R, Navaneeth B (2015) Heterotrophic microalgae cultivation to synergize biodiesel production with waste remediation: progress and perspectives. Bioresour Technol 184:169–178

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Wang Y, Zhang R, Wang W, Xu D, Gou J, Li P, Yu K (2015) Historical levels of the heavy metals reconstructed from sedimentary record in the Hejiang River, located in a typical mining region of Southern China. Sci Total Environ 532:645–654

    Article  CAS  PubMed  Google Scholar 

  • Watanabe K (2001) Microorganisms relevant to bioremediation. Curr Opin Biotechnol 12:237–241

    Article  CAS  PubMed  Google Scholar 

  • Weber DN, Shaw CF, Petering DH (1987) Euglena gracilis cadmium-binding protein-II contains sulfide ion. J Biol Chem 262:6962–6964

    CAS  PubMed  Google Scholar 

  • Wójcik M, Vangronsveld J, Tukiendorf A (2005) Cadmium tolerance in Thlaspi caerulescens: I. Growth parameters, metal accumulation and phytochelatin synthesis in response to cadmium. Environ Exp Bot 53:151–161

    Google Scholar 

  • Wu JS, Ho TC, Chien HC, Wu YJ, Lin SM, Juang RH (2008) Characterization of the high molecular weight Cd-binding complex in water hyacinth (Eichhornia crassipes) when exposed to Cd. J Agric Food Chem 56:5806–5812

    Article  CAS  PubMed  Google Scholar 

  • Yang JL, Zheng SL, He YF, Matsumoto H (2005) Aluminium resistance requires resistance to acid stress: a case study with spinach that exudes oxalate rapidly when exposed to Al stress. J Exp Bot 56:1197–1203

    Article  CAS  PubMed  Google Scholar 

  • Yildiz FH, Davies JP, Grossman AR (1994) Characterization of sulfate transport in Chlamydomonas reinhardtii during sulfur-limited and sulfur-sufficient growth. Plant Physiol 104:981–987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yip B, Rudolph FB (1976) The kinetic mechanism of rat kidney gamma-glutamylcysteine synthetase. J Biol Chem 251:3563–3568

    CAS  PubMed  Google Scholar 

  • Yoshida Y, Tomiyama T, Maruta T, Tomita M, Ishikawa T, Arakawa K (2016) De novo assembly and comparative transcriptome analysis of Euglena gracilis in response to anaerobic conditions. BMC Genomics 17:182

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yoshimoto A, Sato R (1968) Studies on yeast sulfite reductase. I. Purification and characterization. Biochim Biophys Acta 153:555–575

    Article  CAS  PubMed  Google Scholar 

  • Zheng C, Chen M, Tao Z, Zhang L, Zhang XF, Wang JY, Liu J (2015) Different expression of sulfur assimilation pathway genes in Acidithiobacillus ferrooxidans under Cd2+ stress: evidence from transcriptional, enzymatic, and metabolic profiles. Extremophiles 19:429–436

    Article  CAS  PubMed  Google Scholar 

  • Zhu XF, Zheng C, Hu YT, Jiang T, Liu Y, Dong NY, Yang JL, Zheng SJ (2011) Cadmium-induced oxalate secretion from root apex is associated with cadmium exclusion and resistance in Lycopersicon esculentum. Plant Cell Environ 34:1055–1064

    Article  CAS  PubMed  Google Scholar 

  • Zuber H, Davidian JC, Wirtz M, Hell R, Belghazi M, Thompson R, Gallardo K (2010) Sultr4;1 mutant seeds of Arabidopsis have an enhanced sulphate content and modified proteome suggesting metabolic adaptations to altered sulphate compartmentalization. BMC Plant Biol 10:78

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

The present work was partially supported by grants from CONACyT-México (Nos. 107183, 239930, 178638 and 156969) and Instituto de Ciencia y Tecnología del Distrito Federal (No. PICS08-5) to SRE, RMS, ES and RJC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rafael Moreno-Sánchez Ph.D. .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Moreno-Sánchez, R., Rodríguez-Enríquez, S., Jasso-Chávez, R., Saavedra, E., García-García, J.D. (2017). Biochemistry and Physiology of Heavy Metal Resistance and Accumulation in Euglena . In: Schwartzbach, S., Shigeoka, S. (eds) Euglena: Biochemistry, Cell and Molecular Biology. Advances in Experimental Medicine and Biology, vol 979. Springer, Cham. https://doi.org/10.1007/978-3-319-54910-1_6

Download citation

Publish with us

Policies and ethics